Improvement of Neuroenergetics by Hypertonic Lactate Therapy in Patients with Traumatic Brain Injury Is Dependent on Baseline Cerebral Lactate/Pyruvate Ratio

Journal of Neurotrauma

Volumn 33, Issue 7, 2016, Pages 681-687

  Quintard, Hervé ^a,b   Patet, Camille ^a   Zerlauth, Jean Baptiste ^c   Suys, Tamarah ^a   Bouzat, Pierre ^a,d   Pellerin, Luc ^e   Meuli, Reto ^c   Magistretti, Pierre J ^c,f,g   Oddo, Mauro ^a,c  

^a Neuroscience Critical Care Research Group   (Switzerland)

^b UNIVERSITY HOSPITAL OF NICE   (France)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^d GRENOBLE UNIVERSITY HOSPITAL   (France)

^e UNIVERSITY OF LAUSANNE   (Switzerland)

^f KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^g EPFL   (Switzerland)

Author keywords

cerebral blood flow; cerebral microdialysis; hypertonic; lactate; traumatic brain injury

Indexed keywords

IOHEXOL; LACTATE SODIUM; GLUCOSE BLOOD LEVEL; LACTIC ACID; PYRUVIC ACID;

ADULT; ANALYTICAL PARAMETERS; ARTERIAL BLOOD; ARTICLE; BRAIN BLOOD FLOW; BRAIN BLOOD VOLUME; BRAIN METABOLISM; CLINICAL ARTICLE; COMPUTED TOMOGRAPHY SCANNER; CONTINUOUS INFUSION; DRUG EFFICACY; GLASGOW COMA SCALE; HUMAN; INTERVENTION STUDY; LACTATE PYRUVATE RATIO; LIMIT OF QUANTITATION; MULTIDETECTOR COMPUTED TOMOGRAPHY; NEUROIMAGING; PROSPECTIVE STUDY; THREE DIMENSIONAL IMAGING; TRAUMATIC BRAIN INJURY; BRAIN INJURIES, TRAUMATIC; CLINICAL TRIAL; DRUG EFFECTS; ENERGY METABOLISM; FEMALE; GLUCOSE BLOOD LEVEL; INTRAVENOUS DRUG ADMINISTRATION; MALE; METABOLISM; MICRODIALYSIS; MIDDLE AGED; PHYSIOLOGY; X-RAY COMPUTED TOMOGRAPHY; YOUNG ADULT;

ADULT; BLOOD GLUCOSE; BRAIN INJURIES, TRAUMATIC; ENERGY METABOLISM; FEMALE; HUMANS; IMAGING, THREE-DIMENSIONAL; INFUSIONS, INTRAVENOUS; LACTIC ACID; MALE; MICRODIALYSIS; MIDDLE AGED; PROSPECTIVE STUDIES; PYRUVIC ACID; SODIUM LACTATE; TOMOGRAPHY, X-RAY COMPUTED; YOUNG ADULT;

EID: 84964797279     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2015.4057     Document Type: Article

References (43)

1. Glenn, T.C., Kelly, D.F., Boscardin, W.J., McArthur, D.L., Vespa, P., Oertel, M., Hovda, D.A., Bergsneider, M., Hillered, L., and Martin, N.A. (2003). Energy dysfunction as a predictor of outcome after moderate or severe head injury: indices of oxygen, glucose, and lactate metabolism. J. Cereb. Blood Flow Metab. 23, 1239-1250.
2. Vespa, P.M., McArthur, D., O'Phelan, K., Glenn, T., Etchepare, M., Kelly, D., Bergsneider, M., Martin, N.A., and Hovda, D.A. (2003). Persistently low extracellular glucose correlates with poor outcome 6 months after human traumatic brain injury despite a lack of increased lactate: a microdialysis study. J. Cereb. Blood Flow Metab. 23, 865-877.
3. Mergenthaler, P., Lindauer, U., Dienel, G.A., and Meisel, A. (2013). Sugar for the brain: the role of glucose in physiological and pathological brain function. Trends Neurosci. 36, 587-597.
4. Pellerin, L., and Magistretti, P.J. (2012). Sweet sixteen for ANLS. J. Cereb. Blood Flow Metab. 32, 1152-1166.
5. Barros, L.F. (2013). Metabolic signaling by lactate in the brain. Trends Neurosci. 36, 396-404.
6. Ichai, C., Payen, J.F., Orban, J.C., Quintard, H., Roth, H., Legrand, R., Francony, G., and Leverve, X.M. (2013). Half-molar sodium lactate infusion to prevent intracranial hypertensive episodes in severe traumatic brain injured patients: a randomized controlled trial. Intensive Care Med. 39, 1413-1422.
7. Ichai, C., Armando, G., Orban, J.C., Berthier, F., Rami, L., Samat-Long, C., Grimaud, D., and Leverve, X. (2009). Sodium lactate versus mannitol in the treatment of intracranial hypertensive episodes in severe traumatic brain-injured patients. Intensive Care Med. 35, 471-479.
8. Bouzat, P., Sala, N., Suys, T., Zerlauth, J.B., Marques-Vidal, P., Feihl, F., Bloch, J., Messerer, M., Levivier, M., Meuli, R., Magistretti, P.J., and Oddo, M. (2014). Cerebral metabolic effects of exogenous lactate supplementation on the injured human brain. Intensive Care Med. 40, 412-421.
9. Reinstrup, P., Stahl, N., Mellergard, P., Uski, T., Ungerstedt, U., and Nordstrom, C.H. (2000). Intracerebral microdialysis in clinical practice: baseline values for chemical markers during wakefulness, anesthesia, and neurosurgery. Neurosurgery 47, 701-709; discussion 709-710.
10. Timofeev, I., Carpenter, K.L., Nortje, J., Al-Rawi, P.G., O'Connell, M.T., Czosnyka, M., Smielewski, P., Pickard, J.D., Menon, D.K., Kirkpatrick, P.J., Gupta, A.K., and Hutchinson, P.J. (2011). Cerebral extracellular chemistry and outcome following traumatic brain injury: a microdialysis study of 223 patients. Brain 134, 484-494.
11. Bouzat, P., and Oddo, M. (2014). Lactate and the injured brain: friend or foe? Curr. Opinion Crit. Care 20, 133-140.
12. Berthet, C., Castillo, X., Magistretti, P.J., and Hirt, L. (2012). New evidence of neuroprotection by lactate after transient focal cerebral ischaemia: extended benefit after intracerebroventricular injection and efficacy of intravenous administration. Cerebrovasc. Dis. 34, 329-335.
13. Berthet, C., Lei, H., Thevenet, J., Gruetter, R., Magistretti, P.J., and Hirt, L. (2009). Neuroprotective role of lactate after cerebral ischemia. J. Cereb. Blood Flow Metab. 29, 1780-1789.
14. Sala, N., Suys, T., Zerlauth, J.B., Bouzat, P., Messerer, M., Bloch, J., Levivier, M., Magistretti, P.J., Meuli, R., and Oddo, M. (2013). Cerebral extracellular lactate increase is predominantly nonischemic in patients with severe traumatic brain injury. J. Cereb. Blood Flow Metab. 33, 1815-1822.
15. Wintermark, M., van Melle, G., Schnyder, P., Revelly, J.P., Porchet, F., Regli, L., Meuli, R., Maeder, P., and Chiolero, R. (2004). Admission perfusion CT: prognostic value in patients with severe head trauma. Radiology 232, 211-220.
16. Bouzat, P., Marques-Vidal, P., Zerlauth, J.B., Sala, N., Suys, T., Schoettker, P., Bloch, J., Daniel, R.T., Levivier, M., Meuli, R., and Oddo, M. (2015). Accuracy of brain multimodal monitoring to detect cerebral hypoperfusion after traumatic brain injury. Crit. Care Med. 43, 445-452.
17. Dalsgaard, M.K., Quistorff, B., Danielsen, E.R., Selmer, C., Vogelsang, T., and Secher, N.H. (2004). A reduced cerebral metabolic ratio in exercise reflects metabolism and not accumulation of lactate within the human brain. J. Physiology 554, 571-578.
18. Quistorff, B., Secher, N.H., and Van Lieshout, J.J. (2008). Lactate fuels the human brain during exercise. F.A.S.E.B. J. 22, 3443-3449.
19. van Hall, G., Stromstad, M., Rasmussen, P., Jans, O., Zaar, M., Gam, C., Quistorff, B., Secher, N.H., and Nielsen, H.B. (2009). Blood lactate is an important energy source for the human brain. J. Cereb. Blood Flow Metab. 29, 1121-1129.
20. Levy, B., Gibot, S., Franck, P., Cravoisy, A., and Bollaert, P.E. (2005). Relation between muscle Na+K+ ATPase activity and raised lactate concentrations in septic shock: a prospective study. Lancet 365, 871-875.
21. Glenn, T.C., Martin, N.A., McArthur, D.L., Hovda, D., Vespa, P.M.M., Horning, M.A., Johnson, M.L., and Brooks, G.A. (2015). Endogenous nutritive support following traumatic brain injury: peripheral lactate production for glucose supply via gluconeogenesis. J. Neurotrauma 32, 820-832.
22. Simpson, I.A., Carruthers, A., and Vannucci, S.J. (2007). Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J. Cereb. Blood Flow M. 27, 1766-1791.
23. Bergsneider, M., Hovda, D.A., Shalmon, E., Kelly, D.F., Vespa, P.M., Martin, N.A., Phelps, M.E., McArthur, D.L., Caron, M.J., Kraus, J.F., and Becker, D.P. (1997). Cerebral hyperglycolysis following severe traumatic brain injury in humans: a positron emission tomography study. J. Neurosurgery 86, 241-251.
24. Vespa, P., McArthur, D.L., Stein, N., Huang, S.C., Shao, W., Filippou, M., Etchepare, M., Glenn, T., and Hovda, D.A. (2012). Tight glycemic control increases metabolic distress in traumatic brain injury: a randomized controlled within-subjects trial. Crit. Care Med. 40, 1923-1929.
25. Maas, A.I., Stocchetti, N., and Bullock, R. (2008). Moderate and severe traumatic brain injury in adults. Lancet. Neurology 7, 728-741.
26. Bouzat, P., Sala, N., Payen, J.F., and Oddo, M. (2013). Beyond intracranial pressure: optimization of cerebral blood flow, oxygen, and substrate delivery after traumatic brain injury. Ann. Intensive Care 3, 23.
27. Patet, C., Quintard, H., Suys, T., Bloch, J., Daniel, R., Pellerin, L., Magistretti, P., and Oddo, M. (2015). Neuroenergetic response to prolonged cerebral glucose depletion after severe brain injury and the role of lactate. J. Neurotrauma 32, 1560-1566.
28. Bouzier-Sore, A.K., Voisin, P., Canioni, P., Magistretti, P.J., and Pellerin, L. (2003). Lactate is a preferential oxidative energy substrate over glucose for neurons in culture. J. Cereb. Blood Flow Metab. 23, 1298-1306.
29. Cater, H.L., Benham, C.D., and Sundstrom, L.E. (2001). Neuroprotective role of monocarboxylate transport during glucose deprivation in slice cultures of rat hippocampus. J. Physiology 531, 459-466.
30. Schurr, A., Payne, R.S., Miller, J.J., and Rigor, B.M. (1997). Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia: further in vitro validation. J. Neurochemistry 69, 423-426.
31. Yang, J., Ruchti, E., Petit, J.M., Jourdain, P., Grenningloh, G., Allaman, I., and Magistretti, P.J. (2014). Lactate promotes plasticity gene expression by potentiating NMDA signaling in neurons. Proc. Natl. Acad. Sci. U. S. A. 111, 12228-12233.
32. Gallagher, C.N., Carpenter, K.L., Grice, P., Howe, D.J., Mason, A., Timofeev, I., Menon, D.K., Kirkpatrick, P.J., Pickard, J.D., Sutherland, G.R., and Hutchinson, P.J. (2009). The human brain utilizes lactate via the tricarboxylic acid cycle: a 13C-labelled microdialysis and high-resolution nuclear magnetic resonance study. Brain 132, 2839-2849.
33. Boumezbeur, F., Petersen, K.F., Cline, G.W., Mason, G.F., Behar, K.L., Shulman, G.I., and Rothman, D.L. (2010). The contribution of blood lactate to brain energy metabolism in humans measured by dynamic 13C nuclear magnetic resonance spectroscopy. J. Neuroscience 30, 13983-13991.
34. Smith, D., Pernet, A., Hallett, W.A., Bingham, E., Marsden, P.K., and Amiel, S.A. (2003). Lactate: a preferred fuel for human brain metabolism in vivo. J. Cereb. Blood Flow Metab. 23, 658-664.
35. Maran, A., Crepaldi, C., Trupiani, S., Lucca, T., Jori, E., Macdonald, I.A., Tiengo, A., Avogaro, A., and Del Prato, S. (2000). Brain function rescue effect of lactate following hypoglycaemia is not an adaptation process in both normal and type I diabetic subjects. Diabetologia 43, 733-741.
36. Herzog, R.I., Jiang, L., Herman, P., Zhao, C., Sanganahalli, B.G., Mason, G.F., Hyder, F., Rothman, D.L., Sherwin, R.S., and Behar, K.L. (2013). Lactate preserves neuronal metabolism and function following antecedent recurrent hypoglycemia. J. Clin. Invest. 123, 1988-1998.
37. Rice, A.C., Zsoldos, R., Chen, T., Wilson, M.S., Alessandri, B., Hamm, R.J., and Bullock, M.R. (2002). Lactate administration attenuates cognitive deficits following traumatic brain injury. Brain Res. 928, 156-159.
38. Ros, J., Pecinska, N., Alessandri, B., Landolt, H., and Fillenz, M. (2001). Lactate reduces glutamate-induced neurotoxicity in rat cortex. J. Neurosci. Res. 66, 790-794.
39. Rosafio, K., and Pellerin, L. (2014). Oxygen tension controls the expression of the monocarboxylate transporter MCT4 in cultured mouse cortical astrocytes via a hypoxia-inducible factor-1alpha-mediated transcriptional regulation. Glia 62, 477-490.
40. Sotelo-Hitschfeld, T., Fernandez-Moncada, I., and Barros, L.F. (2012). Acute feedback control of astrocytic glycolysis by lactate. Glia 60, 674-680.
41. Jalloh, I., Carpenter, K.L., Grice, P., Howe, D.J., Mason, A., Gallagher, C.N., Helmy, A., Murphy, M.P., Menon, D.K., Carpenter, T.A., Pickard, J.D., and Hutchinson, P.J. (2015). Glycolysis and the pentose phosphate pathway after human traumatic brain injury: microdialysis studies using 1,2-(13)C2 glucose. J. Cereb. Blood Flow Metab. 35, 111-120.
42. Wintermark, M., Thiran, J.P., Maeder, P., Schnyder, P., and Meuli, R. (2001). Simultaneous measurement of regional cerebral blood flow by perfusion CT and stable xenon CT: a validation study. A.J.N.R. 22, 905-914.
43. Vespa, P., Bergsneider, M., Hattori, N., Wu, H.M., Huang, S.C., Martin, N.A., Glenn, T.C., McArthur, D.L., and Hovda, D.A. (2005). Metabolic crisis without brain ischemia is common after traumatic brain injury: a combined microdialysis and positron emission tomography study. J. Cereb. Blood Flow Metabolism 25, 763-774.